REVIEW
published: 20 December 2018
Edited by:
Scott Atran,
Center for the National Scientific
Research (CNRS), France
Reviewed by:
Todd K. Shackelford,
Oakland University, United States
Randolph Nesse,
Arizona State University, United States
*Correspondence:
Robert M. Sapolsky
sapolsky@stanford.edu
Specialty section:
This article was submitted to
Decision Neuroscience,
a section of the journal
Frontiers in Psychology
Received: 13 November 2018
Accepted: 05 December 2018
Published: 20 December 2018
Citation:
Sapolsky RM (2018) Doubled-Edged
Swords in the Biology of Conflict.
Front. Psychol. 9:2625.
doi: 10.3389/fpsyg.2018.02625
Frontiers in Psychology | www.frontiersin.org
doi: 10.3389/fpsyg.2018.02625
Doubled-Edged Swords in the
Biology of Conflict
Robert M. Sapolsky 1,2*
1
Gilbert Laboratory MC 5020, Departments of Biology, Neurology and Neurological Sciences, and Neurosurgery, Stanford
University, Stanford, CA, United States, 2 Institute of Primate Research, National Museums of Kenya, Nairobi, Kenya
Considerable advances have been made in understanding the biological roots of conflict,
and such understanding requires a multidisciplinary approach, recognizing the relevance
of neurobiological, endocrine, genetic, developmental, and evolutionary perspectives.
With these insights comes the first hints of biological interventions that may mitigate
violence. However, such interventions are typically double-edged swords, with the
potential to foster conflict rather than lessen it. This review constitutes a cautionary note
of being careful of what one wishes for.
Keywords: amygdala, frontal cortex, testosterone, oxytocin, violence
INTRODUCTION
We humans are animals—mammals, Old World primates, apes; in other words, we are nothing
more or less than biological organisms, and everything we do must be viewed in the context of our
biology. This is a truism to anyone in the life sciences, but often seems to border on hegemony
to those in the social sciences. This latter view is due to too narrow of a read of what “biology”
means in the context of human behavior (a narrowness, it should be noted, propagated by many a
life scientist). Little will be understood about humans if scientists proclaim the identification of the
brain region, or the gene, or the hormone or neurotransmitter that supposedly explains everything.
Instead, in order to understand why a human social behavior has occurred, one must factor in
neurobiological events 1 s before, but also endocrine events from days before, neuroplasticity
from weeks before, epigenetic events in childhood, fetal environment, the genome in a fertilized
egg, culture, ecology, and evolution. We cannot understand human behavior outside this broad
context of biology; at the same time, that very broadness means that such biology is intimately and
symmetrically intertwined with the traditional domains of social science.
Research concerning the underpinnings of human social behavior has expanded enormously
among neuroscientists, endocrinologists, geneticists, evolutionary biologists, and so on. As one
measure of this expanding interest, the annual meeting of the Society for Neuroscience consistently
attracts more than 30,000 researchers. A growing focus of such research has been on the biology
of conflict, and much has been found out. And not for the first time, with the increase in
understanding of a problem comes the desire to intervene and to correct. This can work wonders in
areas ranging from vaccine development and surgery on fetuses to the fact that there are people who
know how to fix cars. But the study of the biology of human behavior is no less vulnerable to fads
and bandwagons than many other ventures, and they have certainly emerged with respect to the
biology of conflict. This subject is rife with the law of unintended consequences, where one should,
in effect, be careful of what is wished for. This non-technical review considers some realms where
seemingly straightforward biological features of human conflict are anything but straightforward,
producing a number of double-edged swords for those who contemplate interventions. The tone
throughout, in touching on some of the more notable neurobiological domains that are filled with
promise, will be one of caution, where an overabundance of enthusiasm may be unwarranted.
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THE PROMISE OF NEUROPLASTICITY
The first years of life are obviously critical to the sort of brains
we possess as adults; however, such importance can readily lead
to the incorrect conclusion that the trajectory of the brain is set
in stone early in life (Bruer, 2002). Instead, at all stages of life,
the brain can change in response to experience. Few domains of
neuroscience have so fueled excitement, among scientists, and
non-scientists alike, than the promise of such “neuroplasticity”
(Doidge, 2007).
Neuroplasticity in the brain plays out on a variety of levels.
The most fundamental version has been recognized for half a
century, and concerns synapses, the connections by which one
neuron communicates with another. Excitation in one neuron
(an “action potential”) is not guaranteed to similarly excite the
next neuron in line, and repeated stimulation of a particular
synapse leads it to be “strengthened,” which is to say that
excitation in one neuron is now more likely to be propagated to
the next in line. This potentiation of such pre-existing synapses
has long been viewed as one of the fundamental ways by which
learning occurs.
Neuroplasticity occurs on a larger scale as well. New synapses
will form and others retract in response to experience. Axons
and dendrites, the cables by which neurons reach out to other
neurons and form synapses with them, can sprout new branches
and retract old ones. If someone becomes a serious musician,
sprouting occurs such that the amount of space devoted in
the auditory cortex to the sound of his instrument expands
(Pantev and Herholz, 2011); if a volunteer is blindfolded for
days, projection fields into the cortex expand so that the
acuity of other senses increases as a compensation (Merabet
and Pascual-Leone, 2010). As one of the biggest revolutions
in decades in neuroscience, dogma has been overturned with
the demonstration that the adult brain can make new neurons
(Kempermann et al., 2018) (although the extent of it in the
human brain has been questioned recently Sorrells et al., 2018).
Moreover, such “adult neurogenesis” occurs in response to
stimulation, exercise, and as reparative compensation in the
injured brain. As a result of changes in neuron number, synapse
number and complexity of circuitry, entire regions of the brain
can change in size. Become a London cab driver, which demands
forming a complex spatial map of every street and building in
the city, and the part of the brain most responsible for this, the
hippocampus, enlarges (Maguire et al., 2000). If a monkey is
moved into a larger social group than its current one, his frontal
cortex will grow larger, particularly so if he rises high in the
dominance hierarchy (Sallet et al., 2011).
The potential for neuroplasticity readily fuels enormous
optimism—with informed harnessing of these processes,
everything is possible, from coaxing severed spines into
reconnecting to turning the neural circuitry of hate into love
(see Cortright, 2015, for an example of particularly unbridled
enthusiasm in this regard). And here is where double-edged
swords come in. As an example within a narrow neurological
framework, new neurons will be born in the hippocampus after
a hypoxic injury, certainly a good thing in principle; however, a
newly-born neuron attempting to integrate into the pre-exiting
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Double-Edged Swords and Conflict
circuits of an adult brain is a different proposition than in
a fetal brain, and mis-wiring in the former can produce the
self-stimulating loops that generate seizures (Parent et al., 2006).
The double-edge to neuroplasticity is clear when it comes to
the behavioral concerns of this review. Neural plasticity allows
the hippocampus to enlarge, enhancing spatial memory skills.
But at the same time, the same neurobiology allows the amygdala,
a brain region central to fear, to enlarge and contribute to the
crippling state that constitutes post-traumatic stress disorder.
Similarly, the same neural plasticity that underlies the conversion
of a Them to an Us, mediating reconciliation and forgiveness,
makes possible the conversion of an Us to a Them. The plasticity
that allows individuation and perspective-taking to begin to elicit
empathy for a Them is similar to how stress and fear can blunt
the neural capacity for empathy. After all, physiologically, the
opposite of love is indifference rather than hate, and learning to
love and learning to hate are both contingent on the neurobiology
of learning. In other words, neuroplasticity is value-free, and a
new or newly strengthened synapse can be for the better or worse.
THE PROMISE OF EMPATHIC MIRROR
NEURONS
Both neuroscientists and the general public have been fascinated
by “mirror neurons.” The core findings concerning them
are far from the focus of this paper: when we are intent
on performing a particular movement, Movement X, a particular
array of neurons in the “pre-motor cortex” activate in
anticipation of the movement, soon followed by activation
of a cognate array of neurons in the “motor cortex,” which
then commands muscles to actually carry out the behavior.
As first described in the 1990s, about 10% of the pre-motor
neurons that would activate when one is about to make
Movement X activate as well when observing someone else doing
Movement X (Rizzolatti et al., 1996).
The activity of these “mirror neurons” can be remarkably
sophisticated. For example, some neurons that cause Movement
X will activate as mirror neurons when an individual is merely
hearing the sound of someone else doing Movement X. Or
consider Movement X consisting of lifting a tea cup from a
table; different subsets of Movement X neurons will serve as
mirror neurons when observing the cup being lifted in order to
drink from it, vs. being lifted to clear the table (Rizzolatti and
Craighero, 2004). Thus, mirror neurons can encode intent. When
we watch a performer on a tightrope and unconsciously stick our
arms out to stabilize our own balance, this occurs because mirror
neuron activity in the pre-motor cortex was strong enough to
activate neurons in the motor cortex, producing actual behavior.
Most in the field agree that mirror neurons are central to
observational learning. This is both to mimic a behavior, as in
a choreographer demonstrating a movement for the dancers,
and as in learning that, for example, an object should not
be touched by watching someone else leap back in pain after
having done so (Molenberghs et al., 2009). Feverish debate
has emerged with speculation that mirror-like neurons exist in
other cortical regions, and are responsible for understanding
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what someone else is thinking, and for being capable of taking
their perspective (Gallese and Goldman, 1998). Even more
controversial has been the speculation that such neurons are
also responsible for us understanding what someone else is
feeling—the neurobiological substrate of feeling someone else’s
pain (Kaplan and Iacoboni, 2006) [and the speculation that
mirror neurons aid understanding other people’s thoughts and
feelings has prompted the “broken mirror” theory of autism
(Hamilton, 2013)].
The possibility that mirror neurons mediate empathy has
caused tremendous excitement, including among neuroscientists
[one of whom, an eminent figure in the field, has stated “Mirror
neurons will do for psychology what DNA did for biology,” and
has even called these cells “Gandhi neurons” (Ramachandran,
2000)]. This suggests a prescription of more mirror neuron-ing
in our empathy-starved world. However, there is a double-edged
sword in a prescription of enhancing mirror neuron-mediated
empathy; as an example that dominated American news in recent
months, one can feel empathy for a woman whose claim of having
been assaulted you believe, or feel empathy for a man whose claim
of being falsely accused you believe.
More importantly, the biggest problem with mirror neurons
and empathy is in the use of the word “putative” in the previous
sentence. In the quarter century since mirror neurons were first
described, speculation about their role in empathy continues.
However, to date, few to no data exist that actually implicate them
in this role. In the words of one respected psychologist, mirror
neurons are, “the most oversold idea in psychology” (Hickok,
2014).
THE PROMISE OF ADMINISTERING
OXYTOCIN FAR AND WIDE
Brains obviously do not function as islands, and instead are
constantly influenced by sensory stimuli, nutritional status,
bodily states, and so on. Among the most powerful modulators
of brain function are hormones. Particular hormones are secreted
from particular glands (e.g., estrogen from the ovaries), circulate
in the bloodstream, and alter the function of cells throughout the
body; of great importance, cells altered by hormones includes
neurons in the brain. For example, the epinephrine that is
secreted from the adrenals if one were being chased by a lion,
not only promotes the delivery of energy from the liver to thigh
muscles, but also causes the brain to focus and concentrate.
Few hormones are as interesting to a review such as this as
is oxytocin. The hormone, secreted from the pituitary gland,
is responsible for mother-infant bonding among mammals,
an evolutionary development of obvious adaptive advantage.
Moreover, in the relatively few mammalian species that
show stable monogamy, oxytocin mediates the formation and
maintenance of pair bonds (Donaldson and Young, 2008). As a
recent finding, oxytocin is secreted by both dogs and their owners
in response to them making eye contact, and boosting oxytocin
levels prolongs the eye contact (Nagasawa et al., 2015); this is
remarkable, in that this hormone, which has been promoting
mother-infant bonding for 60 million years has, in the last few
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Double-Edged Swords and Conflict
tens of thousands of years of dog domestication, been co-opted
for this novel role.
Most importantly, oxytocin promotes pro-social behavior in a
variety of ways. In both laboratory experiments and naturalistic
settings, it makes people more trusting, forgiving, empathic and
charitable. It improves the accuracy of reading people’s emotions.
Moreover, oxytocin makes people more responsive to social cues
and social feedback (Meyer-Lindenberg et al., 2011).
These pro-social effects prompt easy speculations about the
benefits of administering oxytocin to humans. Which is where
this hormone’s double-edged sword emerges. Excellent recent
work has shown that oxytocin does indeed promote pro-social
behavior, but crucially, only toward in-group members. In
contrast, when dealing with out-group members or strangers,
oxytocin’s effects are the opposite. In such settings, the hormone
decreases trust, and enhances envy and gloating for the successes
and failures, respectively, of the out-group member. Moreover,
the hormone makes people more pre-emptively aggressive to
out-group members, and enhances unconscious biases toward
them (De Dreu et al., 2011a,b; De Dreu, 2012). In other words,
a hormone touted for its capacity to enhance pro-sociality
does no such thing. Instead, what it does is worsen Us/Them
dichotomies, enhancing in-group parochialism as well as out-
group xenophobia. This is certainly not the hormone to cure our
ills.
THE PROMISES OF BANISHING
TESTOSTERONE AND, AS LONG AS
WE’RE AT IT, MALES
A revisionist picture also applies to testosterone, the biological
factor probably most immediately associated with violence – after
all, in the vast majority of social species, and in every culture
examined, males are more likely to be aggressive than females.
Moreover, as something of a gold standard in endocrinology,
subtraction of the hormone (i.e., through surgical or chemical
castration) decreases average levels of aggression in humans
and other mammals. Finally, if testosterone-like androgens are
administered in high amounts (for example, as among athletes
who are steroid abusers), levels of aggression typically rise.
The malign effects of testosterone run even deeper, if more
subtly than that. The hormone decreases trust and biases people
to perceive neutral faces or circumstances as threatening, thus
lowering the threshold for provocation. Empathy is inhibited as
well, and the accuracy of Theory of Mind about other people’s
thinking declines. Testosterone also biases toward risk-taking,
makes individuals less sensitive to the typically constraining
effects of negative reinforcement, and less cooperative because
of an exaggerated sense of the importance and accuracy of one’s
thinking (Hermans et al., 2006; Bos et al., 2010, 2012). None of
these effects auger well for reducing interpersonal and intergroup
conflict.
Yet, there is much reason to doubt the importance
of testosterone to violence. To begin, testosterone boosts
spontaneous aggression only when levels are pushed into the
“pharmacological” range (i.e., higher levels than the body
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normally ever generates); within the normal range, individual
differences in testosterone levels do not predict subsequent
levels of aggression (as measured in a variety of species, with a
variety of endpoints) (Archer, 2006). Furthermore, testosterone
does not “cause” aggression. Instead, it amplifies pre-existing
social tendencies toward aggression, increasing the intensity of
amygdaloid excitation once the region is activated, and lowering
the threshold for such activation (Kendrick and Drewett, 1979).
As a behavioral manifestation of this, if a middle-ranking
primate is administered high levels of testosterone, his levels
of aggression typically rise. However, this does not involve his
now threatening higher-ranking individuals; instead, he simply
displaces aggression more often on lower-ranking ones (Dixson
and Herbert, 1977).
Therefore, testosterone amplifies, rather than causes
aggression. Recent work has revealed an even subtler, more
interesting view of the hormone. As originally proposed as the
“challenge hypothesis,” testosterone does not even amplify pre-
existing social tendencies toward aggression. Instead, it amplifies
pre-existing social tendencies toward whatever behaviors are
needed to maintain status when it is being challenged (Wingfield
et al., 1990). For most social mammals, this distinction is
irrelevant, in that aggression is the means by which a male
maintains high status when challenged. In humans, however,
there are many ways to maintain status. For example, consider
auctions for a charitable cause, as bidders compete for alpha
status of conspicuous largesse. This has been explored in some
remarkable studies involving economic games where status
is accrued through generous offers to other players, and by a
reputation for being trustworthy. In such a setting, testosterone
enhances generosity and other pro-social behaviors in players
(Eisenegger et al., 2010; van Honk et al., 2012; Wibral et al.,
2012). In other words, if we suffer from a surfeit of testosterone-
mediated violence, a significant cause lies in the fact that we
reward violence with status so readily.
The complexities concerning testosterone’s actions segue into
a consideration of the complexities of males in group. Within a
troop of savanna baboons, there is typically high rates of escalated
male-male aggression, something that dominates everyday life.
In contrast, levels of male-male aggression within a group of
chimpanzees are typically lower. The explanation lies in the
differing life histories of baboons and chimpanzees. Among the
former, males leave their natal troop around puberty, transferring
into another troop; as a result, in any troop, the adult males are
typically unrelated and grew up a scattering of other troops, with
no histories of affiliative or cooperative behaviors with each other.
In contrast, male chimpanzees spend their lives in their natal
group, so that the adult males are often siblings or relatives, or
at least individuals who have known each other since childhood.
This picture of chimpanzee males shows the benefits of male
familiarity and cooperation. Naturally, there is a double-edged
sword, in that chimpanzee males are capable of something that
no baboon males in a troop could ever organize. Specifically,
the male chimpanzees in a group carry out organized and
coordinated “border-patrols,” and will attack and even kill any
male encountered from a neighboring group (Wrangham and
Peterson, 1996). As documented more than once, such killings
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Double-Edged Swords and Conflict
can extend to the point of eradicating all the males in the
adjacent group. A group of males getting along well can be a very
frightening thing for the neighbors.
The phenomenon of related male chimpanzees cooperating
raises an implicit double-edged sword about human cooperation.
A cornerstone of thinking about the evolution of behavior is
the importance of relatedness. Enhancing the number of copies
of one’s genes passed into the next generation is not only
accomplished with individual selection and reproduction, but
also “kin selection,” the aiding of relatives in doing the same. The
extent of such cooperation should vary as a function of the degree
of relatedness, summarized in the famous quip, “I’ll gladly lay
down my life for two brothers or eight cousins.”
A key prerequisite for kin selection is, of course, being able to
recognize how related someone is to you. Among most mammals,
this is accomplished through olfaction, where individuals carry
pheromonal signatures that resemble those in other individuals
as a function of the degree of relatedness. A rodent, for example,
can distinguish between full-, half-siblings, cousins and strangers
based on pheromones. In contrast, the human capacity for
kin recognition through pheromones, or through any innate
mechanism, is minimal, at best. Instead, humans have to think
through who is a relative, relying on memory and reasoning.
Herein lies one of the most defining things about human
sociality, namely that we can feel more related to someone
than we actually are. This capacity for “pseudo-kinship” is at
the root of metaphors for aspects of human sociality without
animal precedent—Christian brotherhoods, college sororities,
father figures, and so on. But more importantly, it helps explain
levels of human cooperation far higher than would be expected
by primate standards, when people are tied together by the
pseudo-kinship of everything from shared nationality or religion
to shared intense partisanship for a sports team.
While the capacity to help a stranger based on an implicit
sense of connectedness (the essence of pseudo-kinship) can make
for a more benevolent world, it obviously can prompt something
far from that as well. This is the militaristic world of “bands
of brothers,” and considering everything from Masai warrior-
class rituals to the basic training of the most technologically
advanced armies, militaries excel at generating pseudo-kinship
among their soldiers. This can produce circumstances that would
be impossible among chimpanzees doing border patrols, namely
a human combatant who shares more genes with his enemy
than with the fellow fighter beside him (for example, a German-
American fighting Nazis during World War II, alongside an
Italian-American buddy).
The double-edge sword of pseudo-kinship is obvious in its
potential to fuel co-operativity in groups of humans intent on
killing other humans. But in addition, virtually of necessity,
pseudo-kinship is accompanied by the human capacity to feel less
related to someone than they really are, distancing an out-group
individual to the point where they implicitly hardly feel human—
pseudo-speciation (Berreby, 2008). History has no shortage of
examples of the propagandistic pseudo-speciation that turns
neighbors of a different religion into “a cancer growing in our
culture,” that allows slaves to be classified as sub-human, or
that leads to the characterization of undocumented people as
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an “infestation” (as has been done by an American president
amid the current immigration debate). Pseudo-speciation is one
domain that seems solely a single-edged sword.
THE PROMISE OF RIDDING US OF
EMOTION, OR RIDDING US OF
CEREBRATION, DEPENDING ON YOUR
TASTE
Neuroscientists have long had to stave off dualism, often from the
lay public, resisting simplistic notions of a dichotomy between
brain and body, or mind and brain. One of the most durable
of these dichotomies is the supposedly separate neurobiological
domains of thought and emotion. As most clearly presented
in neurologist Antonio Damasio’s classic book, Descarte’s Error
(2005), this dichotomy is utterly false.
This can be seen on the neurobiological level. Much of the
brain can be broadly (and, of course, falsely) dichotomized into
two domains. One is the cortex, on the surface, standardly
associated with the most abstract of thought. As might be
expected, while occurring broadly among vertebrates, the cortex
expanded greatly in relative size, evolutionarily, with the
emergence of mammals; in turn, it is proportionately larger,
successively, among primates, and apes and humans. Most
interesting is the frontal cortex, the most recently evolved part
of the human brain, a region that is bigger or arguably more
complex in humans than in any other species. The frontal cortex
has an array of functions that can be broadly summarized as
“allowing us to do the right thing when that is the harder
thing to do.” This includes gratification postponement, long-term
planning, executive decision-making, regulation of emotions,
and impulse control. The frontal cortex is, at first glance, the most
cerebral part of the cerebrum.
In contrast is the “limbic system,” a circuit of brain regions,
located beneath the surface of the cortex. In the early part of the
Twentieth century, this region was termed the rhinencephalon
(“nose brain”), as it received massive inputs in the rodent
brain from the olfactory system; such labeling suggested that
upwards of 40% of the brain was devoted to olfaction. Subsequent
pioneering work showed that this region was, in fact, central
to emotion, and the emotion-vs.-olfaction debate was resolved
with the recognition that for a rodent, whose sensory world
is overwhelmingly olfactory, emotion and olfactory social cues
are inseparable. Much of the complex circuitry in the limbic
system eventually converges on the hypothalamus at the base
of the brain. The hypothalamus, in turn, regulates the release
of hormones such as testosterone, estrogen, progesterone, and
glucocorticoids, as well as regulating evolutionarily ancient
autonomic function, such as blood pressure, heart rate, and body
temperature.
This provided an easy dichotomy, where the limbic system’s
concerns were focused on the ancient base of the brain, providing
the means by which emotion can alter the function of the
body, while the cortex sat, both functionally and anatomically
above it all. In this framework, the only communication between
the cortex and the limbic system was inhibitory projections
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Double-Edged Swords and Conflict
from the former to the latter, reining in imprudent emotional
states. A classic example of this sort of regulation is shown in
neuroimaging studies, where subjects are shown pictures of faces
at nearly subliminal speeds. As a well-replicated finding, if the
face rapidly displayed is that of an other-race individual, there
is typically activation in a fraction of a second of the amygdala,
an archetypal limbic structure. However, if the same experiment
is run with exposure to each face on the order of seconds, the
near instantaneous activation of the amygdala is then followed by
frontal cortical activation, inhibiting amygdaloid activity. This is
the effort seen in most people to suppress racist impulses (Kubota
et al., 2012).
Thus, there is seemingly a stark anatomical and functional
dichotomy between “emotion” and “cognition,” with interactions
taking the form of the latter restraining the former. The falseness
of this can first be seen anatomically, in that while there are the
plentiful projections from the frontal cortex to limbic structures,
there is an equivalent amount of signaling from the limbic system
to the frontal cortex. Much of these projections converge on the
ventromedial prefrontal cortex (vmPFC); the density of these
inputs into the brain region that epitomizes the primacy and
independence of cognition even lead to the heretical assertion by
a renowned neuroanatomist that the vmPFC should be classified
as part of the limbic system (Nauta, 1971). In other words, the
limbic system influences the frontal cortex as much as the reverse.
This limbic influence can be appreciated with two examples.
The first concerns memory. The remembering of facts—names,
dates, images, and so on—seems profoundly cortical and abstract.
Yet, the region of the brain most responsible for starting the
process of remembering such information is the hippocampus, a
structure sitting squarely in the limbic system. And in reflecting,
this makes sense in a way that would be appreciated by Proust,
namely that our most vivid memories are filtered through
emotion. This determines what we remember (e.g., why we
readily recall where we were on 9/11, but recall nothing of
9/10), and how it is remembered (e.g., the renowned inaccuracies
of eyewitness accounts of aversive, dramatic events such as
crimes). Moreover, our understanding of how memories, once
consolidated, are recalled has been enriched by recent insights
that emphasize this point as well. A simplistic picture of the
process involves, in effect, taking a memory off its spot on a
storage shelf, examining it as needed, and then returning it to the
shelf as is. Instead, in a phenomenon called “reconsolidation,” the
process of recalling, examining a memory alters it as a function
of one’s emotional state at the time; the memory placed back on
the shelf can be different from the one first removed from it (Lee
et al., 2017).
The second example of the limbic system shaping frontal
cortical function concerns something whose consequences range
from the everyday disruptive to the tragic, which is that during
times of emotional arousal and stress, judgment and impulse
control are greatly impaired. This will be discussed in the next
section.
An understanding of limbic/frontal cortical interactions raises
the temptation to therapeutically intervene, to alter the nature
of those interactions. And what would constitute a helpful
intervention differs dramatically depending on one’s view of
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human nature and the roots of our societal ills. On one hand is the
stance that the world would be less conflicted and violent if our
behavior was increasingly dominated by the world of the frontal
cortex—by thought, reflection, reasoning, emotional regulation
and impulse control—a view that we are at our best, doing the
right thing in a difficult circumstance, when we think our way to
a moral stance. At the other end of the spectrum is the view that
our best human moments are anchored in emotions, by feeling
what it is like to walk a mile in another’s shoes—by empathy,
compassion and love—and that our finest moments arise from
us feeling our way to a moral stance.
The double-edged quality to either of these propositions can
be appreciated when considering the differing consequences
of damage to either markedly “cerebral” or “emotional” parts
of the brain. The punchline is that neither produces an ideal
human. The first proposition would center on the dorsolateral
prefrontal cortex (dlPFC), central to rational decision-making,
the most recently evolved part of the frontal cortex, the nearest
thing to the brain’s “decider.” Selective damage to the dlPFC
produces an organism (human or otherwise) whose behavior
is dominated by limbic inputs funneled through the vmPFC.
The individual is greatly impaired in planning or gratification
postponement, acts impulsively in ways that can be sexually
or aggressively disinhibited and highly damaging. To use a
word with no basis in modern neuroscience beyond being
metaphorical, this is an individual running entirely on id (Barbey
et al., 2013).
A very different, but equally dysfunctional picture is produced
in individuals with damage to the vmPFC, whose frontal cortex’
deliberations occur in the absence of emotional input. Decisions
are extremely difficult to make, because one lacks the “gut
instinct” of limbic inputs that allows one to imagine how
different outcomes to possible behaviors would feel (Damasio,
2005). There is a detached social inappropriateness; an individual
with vmPFC damage, when meeting someone, might say, for
example, “Hello, I see that you are considerably overweight”
(and when castigated later by a mortified spouse, would respond
with calm puzzlement, asking “What’s wrong with that? It’s
true.”). Moreover, vmPFC damage produces someone who is
pathologically utilitarian, who never hesitates to sacrifice one to
save five, even if the one is a loved one (Bechara et al., 1994;
Thomas et al., 2011).
Thus, the world would be unlikely to be a better place were
we to function solely on thought, or emotion. The subtlety
of the interactions of the two can be seen in a key issue in
empathy research. There can be the temptation to view the
capacity for empathy, to feel someone else’s pain, as a virtue
in and of itself, rather than merely one route by which to
actually act with compassion. However, the transition from
empathic feelings to compassionate actions is by no means
guaranteed, and the disconnect is in the phenomenon of empathy
fatigue—the danger of feeling someone’s pain is that pain is
painful, and if the vicarious pain is sufficiently severe, the pull
becomes to turn away, to end one’s own (empathic) pain. The
more severe the emotional arousal when feeling empathy (for
example, as measured by the increase in heart rate), the less
likely a subject is to act pro-socially. As such, while emotions
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Double-Edged Swords and Conflict
are at the core of empathy, emotional detachment can be
central to acting on empathy (Eisenberg et al., 1994; Bloom,
2014).
The contrast between emotionally based and rationally based
decision making has a strong time component to it. This
distinction maps on to the dichotomy between System 1
and System 2 thinking, summarized by Daniel Kahneman in
Thinking, Fast and Slow (2013), where the former is rapid,
intuitive and emotional, whereas the latter is slow, rational
and deliberative. The workings of both systems have double-
edged qualities when it comes to moral decision-making and
the potential for human conflict. As explored in Joshua Greene’s
Moral Tribes: Emotion, Reason and the Gap Between Us and Them
(2014), social conflict can be grouped into two broad categories.
The first concerns in-group members, where everyone agrees
on the same general moral principles. In such cases, conflict is
typically about an individual who, while theoretically adhering
to those principles, is acting in a selfish manner filled with self-
serving justification and rationalization. Greene terms this the
problem of “Me vs. Us,” and likens this to the classic Tragedy of
the Commons, where the problem is a free-rider in a setting of
in-group cooperation. The second domain of conflict is “Us vs.
Them,” between two groups with mutually contradictory beliefs,
moral stances and senses of unalienable rights. The tragedy there
is what Greene terms one of “commonsense morality,” where the
problem is that each side has a passionately felt, common sense
feeling about their own moral correctness, mistaking parochial
intuition for logic and rationality.
Experimental economics work by David Rand and Greene
(Rand et al., 2012) shows something important. Consider a
“Me vs. Us” situation where an individual can either contribute
their resources to a shared fund benefiting all or exploit the
group’s cooperativeness and selfishly keep the resources for
themselves (while benefiting from everyone else’s contributions
to the group). Under such conditions, Greene and Rand show
that the more rapidly a subject must decide what to do with their
resources, the more pro-socially they act. The same is shown if
they are prompted to think intuitively (by first being prompted
by an interview to discuss a time where an intuitive decision
on their part turned out to be better than a deliberative one
would have been). In contrast, the more time subjects had to
made a decision, or the more they were prompted to “carefully
consider” their decision, the more selfishly they acted. In a world
of in-group interactions, our rapid intuitions are pro-social and
cooperative, and slow rational thought facilitates rationalizing
why you should act selfishly and be an exception to an agreed-
upon value.
The contrast with situations of Us vs. Them is obvious.
Beginning with the amygdaloid response in most subjects in
under 100 ms when seeing the face of an other-race individual,
our most rapid, intuitive and emotional responses to out-
group members tend toward fear, hatred, envy, and disgust.
Pro-sociality toward an out-group member whose external
symbols (e.g., dress, ornamentation) are alien, and whose beliefs
are inaccessible or seem intuitively wrong, requires thought,
perspective-taking, objectivity, and a willingness to perhaps
uncomfortably examine oneself in a mirror.
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Sapolsky
THE PROMISE OF BANISHING STRESS
Few things in physiology better constitute a double-edged sword
than the stress response. With the onset of a stressful event, a
wide range of adaptations are mobilized throughout the body,
much of it built around the activation of the sympathetic
nervous system, with its secretion of epinephrine (aka adrenalin)
and norepinephrine, and the secretion from the adrenals of
glucocorticoids, steroid hormones such as cortisol. If the stressful
event is the sort of acute physical crisis that characterizes the
vast majority of stress among other species (e.g., sprinting to
evade a predator or sprinting after a meal), the stress response
is absolutely central to surviving. But when that same stress
response is chronically activated because of the psychosocial
stress specialized in by humans, the result is an increased risk of
cardiovascular, gastrointestinal, immunological and reproductive
disorders (of note, throughout this section, “acute” stress and
stress responses refers to time courses of seconds to an hour or
two, whereas “chronic” refers to anything from a few hours to
decades) (Sapolsky, 1995).
The dichotomy between the beneficial short-term effects of
the stress response and the deleterious chronic effects extend
to the brain as well. The original focus of research was on
the hippocampus, where an acute stress response enhances
oxygen and glucose delivery, and facilitates memory formation;
in contrast, chronic activation of the stress response (primarily
through the actions of glucocorticoids) impairs memory, and
causes atrophy of hippocampal neurons (McEwen and Sapolsky,
1995). A different sort of dichotomy occurs in the amygdala,
where the acute stress response is central to responding to an
immediate threat, whereas chronic activation causes expansion
of amygdaloid neurons and increased risk of anxiety disorders
(Rodrigues et al., 2009).
In recent years, attention has shifted to the effects of stress
on the frontal cortex, where there is a less clear-cut dichotomy
concerning time course; instead, intense stress of any duration
(or exposure to high levels of glucocorticoids) impairs frontal
function. Working memory is disrupted, judgement is impaired,
and coping strategies become perseverative and unresponsive to
feedback (i.e., people cling to habitual problem solving, even if it
is ineffective) (Young et al., 1999; Lyons et al., 2000; Dias-Ferreira
et al., 2009; Schwabe and Wolf, 2010). This last effect involves
poor cost/benefit analyses that bias in the direction of risk-taking,
and is particularly pronounced in males (Starcke et al., 2008;
Lighthall et al., 2009).
While intense stress decreases the activity of neurons in the
frontal cortex, it activates the amygdala, allowing the latter to
dominate the former (Roozendaal et al., 2004), thus increasing
the odds of impulsive behavior. The results include increased
levels of reactive aggression, (Mikics et al., 2007; Roelofs et al.,
2007; Bertsch et al., 2011). These shifts are particularly striking
when the intense stress or elevated glucocorticoid exposure
is on the scale of weeks or more for laboratory rats. Under
such circumstances, the changes in the amygdala and frontal
cortex actually become structural, as amygdaloid neurons sprout
new processes, enhancing the strength and reach of amygdaloid
circuits and increasing the overall size of the structure (Vyas et al.,
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Double-Edged Swords and Conflict
2002), while the opposite occurs in the frontal cortex (Radley
and Morrison, 2006). These chronic stress effects are particularly
damaging during development. Remarkably, having been raised
under the stressful condition of a low socioeconomic status home
produces five-year olds with elevated levels of glucocorticoids,
and whose frontal cortices are likely to be thinner, less active,
and less capable of regulating emotional behavior than average
(Hackman et al., 2010; Sheridan et al., 2012).
Sustained stress or glucocorticoid exposure makes organisms
less pro-social in additional ways. A number of studies have
shown the rudiments of empathy in other species. Mice, for
example, show a decrease in pain thresholds if in proximity
to another mouse in pain (Langford et al., 2006); importantly,
this pain resonance only occurs if the other mouse is a cage
mate, as opposed to a stranger. The presence of a strange
mouse is stressful, causing glucocorticoid secretion, and if the
glucocorticoid release is blocked, a strange mouse’s pain evokes a
threshold shift as readily when the mouse is a cage mage (Martin
et al., 2015). In other words, stress narrows a mouse’s capacity
for “empathy-like” behavior; moreover, the same glucocorticoid-
dependent phenomenon occurs in humans (Martin et al., 2015).
Stress narrows the concern for others in more ways; for example,
exposing subjects to an experimental social stressor causes them
to make more self-centered moral decisions (Starcke et al., 2011;
Youssef et al., 2012).
Finally, stress also provokes aggression for the simple reason
that aggression reduces stress. A number of things buffer the
stress response during a psychological stressor; for a rat, this
includes running on a running wheel, eating, or gnawing on
wood in frustration. Amid this, one of the most effective buffers
is for the rat to be able to bite another individual (Levine et al.,
1988). Such displacement aggression is a reliable stress reducer
across the animal kingdom. Among baboons, for example, about
half of aggression is displacement aggression, and for the same
dominance rank, the more a baboon tends to displace aggression
after losing a fight, the lower his glucocorticoid levels (Sapolsky
and Ray, 1989). The increase in rates of spousal and child abuse
during times of economic stress is but one of the many examples
of stress-induced displacement aggression in humans.
Thus, stress makes organisms fearful, more egoistic and less
empathic, less likely to think clearly, assess risks accurately,
incorporate new data, or to restrain impulses. In a world filled
with the violent consequences of poor judgment and poor
impulse control, it is tempting to imagine a better world thanks
to neurobiological interventions that block the stress response.
This is not possible from a mundane standpoint of health—
while eliminating the stress response might decrease the risks of
a stress-related degenerative disorder such as atherosclerosis, it
would kill the individual the first time they ran for a bus; the
stress response is essential for life when an organism, human or
otherwise, is dealing with an acute physical demand. Eliminating
the stress response is also undesirable for the important reason
that moderate and transient stress is pleasurable, something
we seek out—stress under such circumstances is what we
call stimulation.
For the purposes of this paper, the strongest reason not to
eliminate the stress-response is because of the double-edged
7 December 2018 | Volume 9 | Article 2625
Sapolsky
nature of its effects on the brain and behavior. The adverse effects
of stress on decision-making and impulse control are value-
free, are “adverse” only in the instrumental and neurobiological
sense. In the middle of a stressful crisis, an EMT may act
in perseverative and impulsive ways, making her ineffectual at
saving lives; blunting the effects of stress and glucocorticoids on
the brain at that time is beneficial. But likewise, in the middle of a
stressful crisis, a sociopathic warlord may act in perseverative and
impulsive ways, making him ineffectual at ethnically cleansing
a village. Eliminating the stress response in that circumstance
would be anything but beneficial.
CONCLUSIONS
This review has considered a variety of areas where advances
in behavioral neuroscience relevant to human conflict have
generated enormous excitement. In each case, seemingly
straightforward interventions prompted by these findings (such
as fostering neuroplasticity, or using oxytocin to promote pro-
sociality) instead come with significant double-edged swords.
The enthusiasm with which some of these findings have garnered
translational, or even therapeutic interest has to make one
worry about the hubristic interventions in the past. Behavioral
neuroscience should long be shadowed by frontal lobotomies,
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Conflict of Interest Statement: The author declares that the research was
conducted in the absence of any commercial or financial relationships that could
be construed as a potential conflict of interest.
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9 December 2018 | Volume 9 | Article 2625